Skip to main content
SpringerLink
Log in

Diazotrophic bacteria associated with banana (Musa spp.).

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Nitrogen-fixing bacteria were isolated from surface sterilized banana (Musa spp.) plants and constituted a minor proportion of banana endophytic bacteria. Some isolates were characterized by alloenzyme profiles, biochemical tests, 16S rRNA and rpoB partial gene sequences, plasmid profiles and plant colonization. A large group of enterobacterial isolates that could not be clearly affiliated, most of them ascribed to group I (with characteristics of Enterobacter cloacae) were the diazotrophs most frequently found in banana. Different Klebsiella spp. and Rhizobiumsp. were identified as well. Klebsiella spp. were isolated from inside the roots and stems of plants grown in the two geographical regions sampled and from tissue culture-derived plantlets. Rhizobium sp. isolates were obtained only from Colima where bananas are grown extensively. Group I isolates and Rhizobium sp. could be re-isolated from surface-sterilized banana derived from tissue culture at five months after inoculation and significant increases in stem and leave fresh weight were obtained with some of the isolates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barraquio W L, Revilla L and Ladha J K 1997 Isolation of endophytic diazotrophic bacteria from wetland rice. Plant Soil 194, 15–24.

    Google Scholar 

  • Bashan Y and de-Bashan L E 2002 Protection of tomato seedlings against infection by Pseudomonas syringae pv. tomato by using the plant growth-promoting bacterium Azospirillum brasilense. Appl. Environ. Microbiol. 68, 2637–2643.

    Google Scholar 

  • Bruce S K, Schick D G, Tanaka L, Jiménez EM and Montgomerie J Z 1981 Selective medium for isolation of Klebsiella pneumoniae. J. Clinical Microbiol. 13, 1114–1116.

    Google Scholar 

  • Cavalcante V and Döbereiner J 1988 A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108, 23–31.

    Google Scholar 

  • Chelius M K and Triplett E W 2000. Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl. Environ. Microbiol. 66, 783–787.

    Google Scholar 

  • Cruz L M, Maltempi de Souza E, Weber O B, Baldani J I, Döbereiner J and Oliveira Pedrosa F 2001 16S ribosomal DNA characterization of nitrogen-fixing bacteria isolated from banana (Musa spp.) and pineapple (Ananas comosus (L.) Merril). Appl. Environ. Microbiol. 67, 2375–2379.

    Google Scholar 

  • Döbereiner J, Marriel I E and Nery M 1976 Ecological distribution of Spirillum lipoferum Beijerinck. Can. J. Microbiol. 22, 1464–1473.

    Google Scholar 

  • de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins M D, Kersteres K, Dreyfus B and Gillis M 1998 Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int. J. Syst. Bacteriol. 4, 1277–1290.

    Google Scholar 

  • Dojka M A, Hugenholtz P, Haack S K and Pace N R 1998 Microbial diversity in a hydrocarbon-and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64, 3869–3877.

    Google Scholar 

  • Dong Y, Glasner J D, Blattner F R and Triplett E W 2001 Genomic interspecies microarray hybridization: rapid discovery of three thousand genes in the maize endophyte, Klebsiella pneumoniae 342, by microarray hybridization with Escherichia coli K-12 Open Reading Frames. Appl. Environ. Microbiol. 67,1911–1921.

    Google Scholar 

  • Drancourt M, Bollet C, Carta A and Rousselier P 2001 Phylogenetic analyses of Klebsiella species delineate Klebsiella and Raoultella gen. nov., with description of Raoultella ornithinolytica comb. nov., Raoultella terrigena comb. nov. and Raoultella planticola comb. nov. Int. J. Syst. Evol. Microbiol. 51, 925–932.

    Google Scholar 

  • Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H and Minamisawa K 2001 Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl. Environ. Microbiol. 67, 5285–5293.

    Google Scholar 

  • Engelhard M, Hurek T and Reinhold-Hurek B 2000 Preferential occurrence of diazotrophic endophytes, Azoarcus spp., in wild rice species and land races of Oryza sativa in comparison with modern races. Environ. Microbiol. 2, 131–141.

    Google Scholar 

  • Fahraeus G 1957 The infection of clover root hair by nodule bacteria studied by a single glass slide technique. J. Gen. Microbiol. 16, 374–381.

    Google Scholar 

  • Fujii T, Huang Y-D, Higashitani A, Nishimura Y, Iyama S, Hirota Y, Yoneyama T and Dixon R A 1987 Effect of inoculation with Klebsiella oxytoca and Enterobacter cloacae on dinitrogen fixation by rice-bacteria associations. Plant Soil 103, 221–226.

    Google Scholar 

  • González-Pasayo R and Martínez-Romero E 2000 Multiresistance genes of Rhizobium etli CFN42. Mol. Plant-Microbe Interact. 13, 572–577.

    Google Scholar 

  • Gough C, Vasse J, Galera C, Webster G, Cocking E and Dénarié J 1997 Interactions between bacterial diazotrophs and non-legume dicots: Arabidopsis thaliana as a model plant. Plant Soil 194, 123–130.

    Google Scholar 

  • Grimont F, Grimont P A D and Richard C 1992 The genus Klebsiella. In The Prokaryotes Second Edition. A Handboook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications. Eds. A Balows, H G Trüper, M Dworkin, W Harder and K-H Schleifer. pp. 2775–2796. Springer-Verlag, New York

    Google Scholar 

  • Gutiérrez-Zamora M L and Martínez-Romero E 2001 Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J. Biotechnol. 91, 117–126.

    Google Scholar 

  • Haque S E and Ghaffar A 1993 Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J. Phytopathol. 138, 157–193.

    Google Scholar 

  • Holland MA and Polacco J C 1994 PPFMs and other covert contaminants: is there more to plant physiology than just plant? Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 197–209.

    Google Scholar 

  • Hynes M F and McGregor N F 1990 Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol. Microbiol. 4, 567–574.

    Google Scholar 

  • James E K 2000 Nitrogen fixation in endophytic and associative symbiosis. Field Crops Res. 65, 197–209.

    Google Scholar 

  • Ladha J K, Barraquio W L and Watanabe I 1983 Isolation and identification of nitrogen-fixing Enterobacter clocae and Klebsiella planticola associated with rice plants. Can. J. Microbiol. 29, 1301–1308.

    Google Scholar 

  • Ladha J K and Reddy P M Eds 2000 The Quest for Nitrogen Fixation in Rice. Proceedings of the Third Working Group Meeting on Assessing Opportunities for Nitrogen Fixation in Rice, 9–12 Aug. 1999. Makati City (Philipines): International Rice Research Institute. Los Baños, Philippines. 359 pp.

  • Leifert C, Ritchie J Y and Waites WM 1991 Contaminants of planttissue and cell cultures. World J. Microbiol. Biotechnol. 7, 452–469.

    Google Scholar 

  • Martínez-Romero E and Rosenblueth M 1990 Increased bean (Phaseolus vulgaris L.) nodulation competitiveness of genetically modified Rhizobium strains. Appl. Environ. Microbiol. 56, 2384–2388.

    Google Scholar 

  • Martínez-Romero E, Segovia L, Mercante F M, Franco A A, Graham P and Pardo M A 1991 Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees.Int. J. Syst. Bacteriol. 41, 417–426.

    Google Scholar 

  • Mirza M S, Ahmad W, Latif F, Haurat J, Bally R, Normand P and Malik K A 2001 Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) onmicro-propagated sugarcane in vitro. Plant Soil 237, 47–54.

    Google Scholar 

  • Mollet C, Drancourt M and Didier R 1997 rpoB sequence analysis as a novel basis for bacterial identification. Mol. Microbiol. 26, 1005–1011.

    Google Scholar 

  • O'Callaghan K J, Davey M R and Cocking E C 1999 Xylem colonization of Sesbania rostrata by Azorhizobium caulinodans ORS571. In Highlights of Nitrogen Fixation Research. Eds E Martínez and G Hernández. pp. 145–147. Kluwer Academic/ Plenum Publishers. New York.

    Google Scholar 

  • O'Callaghan K J, Stone P J, Hu X, Griffiths D W, Davey M R and Cocking E C 2000 Effects of glucosinolates and flavonoids on colonization of the roots of Brassica napus by Azorhizobium caulinodans ORS571. Appl. Environ. Microbiol. 66, 2185–2191.

    Google Scholar 

  • Okon Y and Labandera-González C A 1994 Agronomic aplicactions of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol. Biochem. 26, 1591–1601.

    Google Scholar 

  • Palus J A, Borneman J, Ludden PW and Triplett EW1996A diazotrophic bacterial endophyte isolated from stems of Zea mays L., and Zea luxurians Itlis and Doebley. Plant Soil 186, 135–142.

    Google Scholar 

  • Phillips D A, Joseph C M, Yang G P, Martinez-Romero E, Sanborn J R and Volpin H 1999 Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth Proc. Natl. Acad. Sci. USA 96, 12275–12280.

    Google Scholar 

  • Poly F, Monrozier L J and Bally R 2001 Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res. Microbiol. 152, 95–103.

    Google Scholar 

  • Powledge F 1996 Making the Most of Musa. The role of the International Network for the Improvement of Banana and Plantain. In International Network for the Improvement of Banana and Plantain. Eds C Picq and R Raymond. INIBAP, International Plant Genetic Resources Institute, Montpellier, France.

    Google Scholar 

  • Reinhold B, Hurek T, Niemann E-G and Fendrik I 1986 Close association of Azospirillum and diazotrophic rods with different root zones of Kallar grass. Appl. Environ. Microbiol. 52, 520–526.

    Google Scholar 

  • Reinhold-Hurek B, Hurek T, Gillis M, Hoste B, Vancanneyt M, Kersters K and DeLey J 1993 Azoarcus gen nov., nitrogen-fixing Proteobacteria associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth), and description of two species, Azoarcus indigens sp. nov. and Azoarcus communis sp. nov. Int. J. Syst. Bacteriol. 43, 574–584.

    Google Scholar 

  • Robles-González M M and Orozco-Romero J 1996 Producción de plátano enano gigante mediante la técnica de cultivo de tejidos. Editorial Conexión Gráfica, S. A. de C. V. Guadalajara, México.

    Google Scholar 

  • Rodríguez Cáceres E A 1982 Improved medium for isolation of Azospirillum spp. Appl. Environ. Microbiol. 44, 990–991.

    Google Scholar 

  • Rogel M A, Hernández-Lucas I, Kuykendall L D, Balkwill D L and Martínez-Romero E 2001 Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl. Environ. Microbiol. 67, 3264–3268.

    Google Scholar 

  • Selander R K, Caugant D A, Ochman H, Musser J M, Gilmour M N and Whittam T S 1986 Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51, 873–884.

    Google Scholar 

  • Sturz A V, Christie B R, Matheson B G and Nowak J 1997 Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol. Fertil Soils 25, 13–19.

    Google Scholar 

  • Tien T, Gaskins M H and Hubbell D H 1979 Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl. Environ. Microbiol. 37, 1016–1024.

    Google Scholar 

  • Toledo I, Lloret L and Martínez-Romero E 2003 Sinorhizobium americanum sp nov., a new sinorhizobium species nodulating native Acacia spp. in Mexico. System Appl. Microbiol. 26, 54–64.

    Google Scholar 

  • Wang E T, Rogel M A, García-de los Santos A, Martínez-Romero J, Cevallos M A and Martínez-Romero E 1999 Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int. J. Syst. Bacteriol. 49, 1479–1491.

    Google Scholar 

  • Weber O B, Baldani J I and Döbereiner J 2000 Bactérias diazotróficas em mudas de bananeira. Pesquisa Agropecuária Brasileira. 35, 2227–2285.

    Google Scholar 

  • Weber O B, Baldani V L D, Teixeira K R S, Kirchhof G, Baldani J I and Dobereiner J 1999 Isolation and characterization of diazotrophic bacteria from banana and pineapple plants. Plant Soil 210, 103–113.

    Google Scholar 

  • Weber O B, Cruz L M, Baldani J I and Döbereiner J 2001 Herbaspirillum-like bacteria in banana plants. Braz. J. Microbiol. 32, 201–205.

    Google Scholar 

  • Weisburg WG, Barns S M, Pelletier D A and Lane D J 1991 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173, 697–703.

    Google Scholar 

  • Xi C, Dirix G, Hofkens J, De Schryver F C, Vanderleyden J and Michiels J 2001 Use of dual marker transposons to identify new symbiosis genes in Rhizobium. Microbial. Ecol. 41, 325–332.

    Google Scholar 

  • Yanni Y G, Rizk R Y, Abd El-Fattah F K, Squartini A, Corich V, Giacomini A, De Bruijn F, Rademaker J, Maya-Flores J and Ostrom P 2001 The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Austr. J. Plant Physiol. 28, 845–870.

    Google Scholar 

  • Yanni Y G, Rizk R Y, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stoltzfus J, Buckley D, Schmidt T M, Mateos P F, Ladha J K and Dazzo F B 1997 Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194, 99–114.

    Google Scholar 

  • Young J M, Kuykendall L D, Martínez-Romero E, Kerr A and Sawada H 2001 A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn, 1942 and Allorhizobium undicola de Lajudie et al. (1998) as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int. J. Syst. Evol. Microbiol. 51, 89–103.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centro de Investigación sobre Fijación de Nitrógeno, UNAM, Ap. P. 565-A., Cuernavaca, Mor, México

    Lucía Martínez, Jesús Caballero-Mellado & Esperanza Martínez-Romero

  2. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Km 35 Carretera Colima-Manzanillo, Ap. P. 88, C.P. 28100, Tecomán, Col., México

    José Orozco

Authors
  1. Lucía Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jesús Caballero-Mellado
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Orozco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Esperanza Martínez-Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Esperanza Martínez-Romero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martínez, L., Caballero-Mellado, J., Orozco, J. et al. Diazotrophic bacteria associated with banana (Musa spp.).. Plant and Soil 257, 35–47 (2003). https://doi.org/10.1023/A:1026283311770

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026283311770

Search

Navigation